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Genomic and Transcriptomic Investigations of the Evolutionary Transition from Oviparity to Viviparity

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Genomic and Transcriptomic Investigations of the Evolutionary Transition from Oviparity to Viviparity Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity Wei Gaoa,b,1, Yan-Bo Suna,1, Wei-Wei Zhoua,1, Zi-Jun Xionga,c,1, Luonan Chend,e, Hong Lif, Ting-Ting Fua,b, Kai Xua,b, Wei Xua,b,LiMaf, Yi-Jing Chenf, Xue-Yan Xiangc, Long Zhouc, Tao Zengd, Si Zhangd,g, Jie-Qiong Jina, Hong-Man Chena, Guojie Zhanga,c,e,h, David M. Hillisi,2, Xiang Jif,2, Ya-Ping Zhanga,e,2, and Jing Chea,e,j,2 aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223 Kunming, China; bKunming College of Life Science, University of Chinese Academy of Sciences, 650204 Kunming, China; cChina National Genebank, Beijing Genomics Institute-Shenzhen, 518083 Shenzhen, China; dKey Laboratory of Systems Biology, Center for Excellence in Molecular Cell Science, Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 200031 Shanghai, China; eCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650223 Kunming, China; fJiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, 210023 Nanjing, Jiangsu, China; gSchool of Life Science and Technology, ShanghaiTech University, 201210 Shanghai, China; hSection for Ecology and Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark; iDepartment of Integrative Biology and Biodiversity Center, University of Texas at Austin, Austin, TX 78712; and jSoutheast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, 05282 Nay Pyi Taw, Myanmar Contributed by David M. Hillis, December 11, 2018 (sent for review September 19, 2018; reviewed by Jonathan B. Losos and David D. Pollock) Viviparous (live-bearing) vertebrates have evolved repeatedly 98–129 times (depending on the analysis) in squamates, ac- within otherwise oviparous (egg-laying) clades. Over two-thirds counting for over two-thirds of all origins of viviparity in verte- of these changes in vertebrate reproductive parity mode hap- brates (2–5). In addition, many of these origins of viviparity are pened in squamate reptiles, where the transition has happened evolutionarily recent, as viviparity has arisen in species or pop- between 98 and 129 times. The transition from oviparity to ulations of otherwise oviparous clades. However, the phylogenetic viviparity requires numerous physiological, morphological, and timing of transitions from oviparity to viviparity is not always immunological changes to the female reproductive tract, including clear, and there are some suggestions of rare reversals from eggshell reduction, delayed oviposition, placental development viviparity to oviparity in a few squamate groups; there are for supply of water and nutrition to the embryo by the mother, enhanced gas exchange, and suppression of maternal immune Significance rejection of the embryo. We performed genomic and transcrip- tomic analyses of a closely related oviparous–viviparous pair of The transition from oviparity to viviparity results in greater lizards (Phrynocephalus przewalskii and Phrynocephalus vlangalii) flexibility for parental control of embryonic development, to examine these transitions. Expression patterns of maternal ovi- which in turn allows viviparous organisms to reproduce suc- duct through reproductive development of the egg and embryo cessfully in otherwise adverse environments. These advan- differ markedly between the two species. We found changes in tages have led to numerous origins of viviparity among expression patterns of appropriate genes that account for each of vertebrates. We studied the genetic bases of this transition by the major aspects of the oviparity to viviparity transition. In addi- comparing genomic and transcriptomic data of a closely related tion, we compared the gene sequences in transcriptomes of four oviparous–viviparous pair of lizards (Phrynocephalus prze- oviparous–viviparous pairs of lizards in different genera (Phryno- walskii and Phrynocephalus vlangalii). We identified genes cephalus, Eremias, Scincella, and Sphenomorphus) to look for pos- whose temporal and spatial changes in expression account for sible gene convergence at the sequence level. We discovered low the major physiological, morphological, and immunological levels of convergence in both amino acid replacement and evolu- aspects of the oviparity–viviparity transition. These changes tionary rate shift. This suggests that most of the changes that account for eggshell reduction or degeneration, placental de- produce the oviparity–viviparity transition are changes in gene ex- velopment, delayed oviposition, embryonic attachment, and pression, so occasional reversals to oviparity from viviparity may not inhibited maternal immune rejection of the embryo. be as difficult to achieve as has been previously suggested. Author contributions: W.-W.Z., D.M.H., Y.-P.Z., and J.C. designed research; W.G., Y.-B.S., Phrynocephalus | viviparity | oviparity | convergent evolution | W.-W.Z., L.C., G.Z., D.M.H., X.J., Y.-P.Z., and J.C. managed the project; W.G., W.-W.Z., T.-T.F., temporal–spatial expression K.X., W.X., J.-Q.J., and H.-M.C. conducted field work and performed DNA and RNA ex- periments; W.G., H.L., L.M., Y.-J.C., and X.J. carried out the breeding program and sample collection; Z.-J.X., X.-Y.X., L.Z., and G.Z. performed genome assembly and annotation; iviparity (live-bearing) is a reproductive mode in which W.G., L.C., T.Z., and S.Z. identified genes related to placentation; W.G. and Y.-B.S. per- Vpregnant females maintain developing embryos inside their formed the analysis of convergent evolution; Y.-B.S. performed the analysis of positive selection; W.G. performed transcriptomic expression analysis; and W.G., Y.-B.S., D.M.H., reproductive tracts and give birth directly to offspring (1). In X.J., Y.-P.Z., and J.C. discussed results and wrote the paper. contrast, oviparity (egg-laying) is the reproductive pattern in Reviewers: J.B.L., Washington University in St. Louis; and D.D.P., University of Colorado which females lay eggs that continue to develop independently of Health Sciences Center. the mother until hatching. Viviparity evolves from oviparity Conflict of interest statement: D.D.P. and G.Z. are coauthors on a 2014 paper. through gradual increases in the length of egg retention until Published under the PNAS license. uterine embryogenesis is complete. Viviparous species provide Data deposition: The data have been deposited in the Genome Sequence Achieve, gsa. an environment for embryonic development and protect the big.ac.cn (accession no. CRA001096). The whole-genome sequence data reported in this embryo from environmental threats. The transition between paper have been deposited in the BIGD Genome Warehouse, bigd.big.ac.cn/gwh (acces- sion nos. GWHAAFC00000000 and GWHAAFD00000000) and are also available in the oviparity and viviparity has significant physiological and ecolog- CNGB Nucleotide Sequence Archive, https://db.cngb.org/cnsa (accession no. CNP0000203). ical consequences to the organisms and, as such, the processes 1W.G., Y.-B.S., W.-W.Z., and Z.-J.X. contributed equally to this work. involved in the transition are of general interest. 2To whom correspondence may be addressed. Email: [email protected], zhangyp@mail. Squamate reptiles (lizards, snakes, and amphisbaenians) offer kiz.ac.cn, [email protected], or [email protected]. an ideal model system to study the evolutionary transition from This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. oviparity to viviparity in vertebrates. About 20% of extant 1073/pnas.1816086116/-/DCSupplemental. squamate species are viviparous. Viviparity has evolved between Published online February 11, 2019. 3646–3655 | PNAS | February 26, 2019 | vol. 116 | no. 9 www.pnas.org/cgi/doi/10.1073/pnas.1816086116 Downloaded by guest on September 27, 2021 nonetheless many cases in which the recent transition from oviparity length of 1,415 bp for P. przewalskii and 1,388 bp for P. vlangalii to viviparity is strongly supported (4–9). Comparative studies of (SI Appendix, Table S2). More than 99% of the protein-coding closely related oviparous and viviparous species has confirmed genes of both species were functionally annotated according to that this transition in parity requires a number of physiological, SwissProt and TrEMBL databases (SI Appendix, Table S3). Us- morphological, and immunological changes. These include re- ing the BUSCO database of 3,023 universal single-copy ortho- duced eggshell (10–12), delayed oviposition (11, 13, 14), placental logs found across vertebrates (25), we sequenced 84.4% and development for supply of water and nutrition to the embryo by 87.5% of the expected vertebrate genes in P. przewalskii and the mother (13, 15, 16), enhanced gas exchange (14, 15, 17), and P. vlangalii, respectively (SI Appendix, Table S4). suppression of maternal immune rejection of the embryo (18, 19). However, the specific changes to genes or their expression that Gene-Expression Changes During Uterine Embryogenesis. We eval- result in these major transformations are largely unknown. uated gene expression in the oviduct (Fig. 1A) by sequencing the Recently, a comparative analysis based on restriction-site– transcriptomes of oviducts from preovulation to postoviposition associated DNA data in Zootoca vivipara, a species with both (for the oviparous species) or postparturition (for the viviparous
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